Understanding and Assessing Emotions in Marine Mammals Under Professional Care
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2021, 34 Heather M. Hill Editor Peer-reviewed Understanding and Assessing Emotions in Marine Mammals Under Professional Care Fabienne Delfour and Aviva Charles Parc Astérix, Plailly, France In the last 30 years, concerns about animal emotions have emerged from the general public but also from animal professionals and scientists. Animals are now considered as sentient beings, capable of experiencing emotions such as fear or pleasure. Understanding animals’ emotions is complex and important if we want to guarantee them the best care, management, and welfare. The main objectives of the paper are, first, to give a brief overview of various and contemporary assessments of emotions in animals, then to focus on particular zoo animals, that is, marine mammals, since they have drawn a lot of attention lately in regards of their life under professional care. We discuss here 1 approach to monitor their emotions by examining their laterality to finally conclude the importance of understanding animal emotion from a holistic welfare approach. Keywords: behavior, cetaceans, cognition, emotions, pinnipeds In the three last decades, we have witnessed a growing interest in animal emotions coming from public concerns for animal welfare, welfare scientists, zoologists, neuroscientists, and animal professionals working in zoos for instance. To better overtake the ongoing debate on how to define “emotions”, “feelings”, “moods” and “affective states” (Paul & Mendl, 2018, we suggest reading the recent paper by Kremer et al. (2020) to have a synthetic overview of the field of animal emotion. Here, we use the term “emotions” to be defined as subjective feelings of an individual during a short period of time and, in a particular situation, associated with physical and behavioral changes (Destrez et al., 2013), and described by their positive or negative valence and intensity (Leliveld et al., 2013). Understanding others’ emotions is always challenging and more so in nonhuman animals. In order to understand how emotions manifest themselves in other species, scientists use various approaches and indicators, such as implementing evaluations of emotions in contemporary animal welfare assessment. For instance, Webster (2005) triangulation principle involves three main categories of measures (i.e. physiology, behavior, and cognition) that are also the three components of animals’ emotional responses (Désiré et al., 2002). The aim of the present paper is first to introduce various ways to assess emotions in animals. Then, since zoo animals and more particularly marine mammals’ captivity and welfare are regularly questioned and since cognition is now included in animal welfare assessment, we provide information on studies assessing emotions on those animals under professional care. We also discuss one approach to evaluate emotions by examining laterality. We end by pointing out the importance of understanding animal emotion in the framework of animal welfare. Assessing Emotions in Nonhuman Animals Animals’ Behavioral Postures To assess and understand emotions in nonhuman animals, behavioral postures that might be analogous to facial expressions in humans are valuable for studies of emotion. For instance, sheep (Ovis arie) exposed to suddenness or unfamiliarity test stimuli will negative-contrast position their ears; in a neutral state, ears are horizontal, but they point backward in unfamiliar, unpleasant, and/or uncontrollable situations (fearful situations), whereas the ears point up in controllable negative situations; sheep display asymmetric postures in very sudden situations (Boissy et al., 2011). When looking at different stimuli in the presence of their owner, domestic dogs showed a right-sided bias in the amplitude of tail wagging, and when tested alone or in the Please send correspondence to Fabienne Delfour. Email: [email protected] https://doi.org/10.46867/ijcp.2021.34.00.01 presence of an unfamiliar conspecific, dogs showed a left-sided bias (Quaranta et al., 2007). In pigs, high- frequency lateral tail movement is linked to positive emotions, whereas long-lasting ear movement is linked to a decreased welfare (Rius et al., 2018). Facial expressions are also good indicators of animals’ affective state; for instance, blue-and-yellow macaws (Ara Ararauna) blush and fluff facial feathers in some intraspecific social interactions and interspecific interactions with their caretakers (Bertin, Beraud, et al., 2018). Similar observations were conducted on Japanese quails (Coturnix japonica) showing that, in these birds, variation in crown feather height and pupil area could be indicators of positive emotions (Bertin, Cornilleau, et al., 2018). When being gently groomed, horses (Equus caballus) show a moderately raised neck, extended immobile or twitching upper lips, and backwards pointed ears (Lansade et al., 2018). Vocal Productions Associations between vocal production and emotions are particularly useful in social animals as they modulate social interactions, give information about each other’s intentions, and predict potential behaviors (Briefer, 2012). For instance, in horses, a snort is associated with positive situations and positive affective state postures (ears in forward or sideways positions) and is thus considered a reliable indicator of positive emotions in this species (Stomp et al., 2018). Furthermore, dogs produce vocalizations with shorter durations, wider amplitude range, and smaller frequency modulations in positive (play) contexts than in negative contexts (Goursot et al., 2018). Many social animals emit distress calls in contexts of fear such as danger, injury or illness; these particular vocalizations function to attract attention from others, to warn them of potential danger, to call for help (i.e. alarm), and/or to confuse the predator (Liévin-Bazin et al., 2018; Vannoni et al., 2005; Wu et al., 2018). Cognitive Biases Since emotions cannot be measured directly, scientists use a posteriori measures to postulate on potential emotions felt by animals (Désiré et al., 2002); that is, scientists identify emotions on the basis of the cognitive evaluation of situations by the animal itself (Dantzer, 2002). Cognitive biases describe the effects of emotions on a subject’s cognitive functioning (i.e., judgment, attention, and memory) and are adaptive (Mendl et al., 2009). In other words, they refer to how an individual’s emotional state affects the way it processes information. To study cognitive bias, scientists will usually induce emotional state experimentally by imposing various stressful situations to the animals (i.e., a physical stress; Bateson et al., 2011), a chronic environmental stress (Doyle et al., 2011), or a psychological stress (Rygula et al., 2013) or by using specific pharmacological treatments (Lee et al., 2018). Cognitive bias studies have been conducted on farm and laboratory animals and on pets, as well as a few zoo animal species including three species of primates (Macaca fuscata, Gorilla gorilla and Pan troglodytes; Cronin et al., 2018; McGuire & Vonk, 2018) and an American black bear (Ursus americanus; McGuire et al., 2017). In animals, particularly zoo animals, cognitive bias tests are one of the methods used to assess their welfare (Wolfensohn et al., 2018). Judgment biases are cognitive biases where affect influences judgments about the affective value of stimuli (i.e., positive affect is associated with optimistic judgments and negative affect with pessimistic judgments; Crump et al., 2018). Judgment bias tasks have been built for mammals, birds, and insects (Crump et al., 2018). They require long training periods that could negatively impact the animals’ performances. Attention bias (i.e., preferential allocation of cognitive resources towards one form of information over another; Crump et al., 2018) are good alternatives. They do not require extensive training and do not depend on interpreting pessimistic or optimistic responses. For instance, in a revised version of the emotional Stroop task, rhesus monkeys (Macaca mulatta) that have experienced a stressor (i.e., presumably stressful veterinary exam) slowed their responses to mildly threatening stimuli (i.e., direct gaze) compared to their speed to respond during a baseline period (Bethell et al., 2016). The authors named this response cognitive freeze and urged scientists to consider the response-slowing paradigm. 2 Anticipatory Behavior Anticipatory behavior is defined as an activity performed by an individual in expectation of a predictable upcoming event (Spruijt et al., 2001) and is expressed by an increased activity, vigilance, and/or increased transitions between two successive behaviors (van den Bos et al., 2003). Expected events could be feeding events (Martini et al., 2018), play opportunities (Anderson et al., 2015), socio-sexual activities (Van der Harst et al., 2003), and positive and enjoyable human-animal interactions (Krebs et al., 2017). Since anticipatory behavior is linked to the reward sensitivity system (Van der Harst & Spruijt, 2007), animals experiencing negative affective states will put more incentive value on acquiring positive rewards and will more intensively anticipate their arrival. Alternatively, anticipatory behaviors can give information on the individual’s motivation and the way rewards are valued. In that case, they are known to enhance positive affective states/emotions, such as excitation (Clegg et al., 2018). Even if the link between anticipatory behavior and affective state is not that simple, it is a valid